% IMPORTANT: The following is UTF-8 encoded. This means that in the presence
% of non-ASCII characters, it will not work with BibTeX 0.99 or older.
% Instead, you should use an up-to-date BibTeX implementation like “bibtex8” or
% “biber”.
@ARTICLE{Andrzejak:164003,
author = {Andrzejak, Ewa Izabella and Rabinovitch, Eshed and Kreye,
Jakob and Prüss, Harald and Rosenmund, Christian and Ziv,
Noam E and Garner, Craig Curtis and Ackermann, Frauke},
title = {{P}atient-{D}erived {A}nti-{NMDAR} {A}ntibody {D}isinhibits
{C}ortical {N}euronal {N}etworks through {D}ysfunction of
{I}nhibitory {N}euron {O}utput.},
journal = {The journal of neuroscience},
volume = {42},
number = {15},
issn = {0270-6474},
address = {Washington, DC},
publisher = {Soc.},
reportid = {DZNE-2022-00672},
pages = {3253-3270},
year = {2022},
note = {(CC BY)},
abstract = {Anti-NMDA receptor (NMDAR) encephalitis is a severe
neuropsychiatric disorder associated with autoantibodies
against NMDARs, which cause a variety of symptoms from
prominent psychiatric and cognitive manifestations to
seizures and autonomic instability. Previous studies mainly
focused on hippocampal effects of these autoantibodies,
helping to explain mechanistic causes for cognitive
impairment. However, antibodies' effects on higher cortical
network function, where they could contribute to psychosis
and/or seizures, have not been explored in detail until now.
Here, we employed a patient-derived monoclonal antibody
targeting the NR1 subunit of NMDAR and tested its effects on
in vitro cultures of rodent cortical neurons, using imaging
and electrophysiological techniques. We report that this
hNR1 antibody drives cortical networks to a hyperexcitable
state and disrupts mechanisms stabilizing network activity
such as Npas4 signaling. Network hyperactivity is in part a
result of a reduced synaptic output of inhibitory neurons,
as indicated by a decreased inhibitory drive and levels of
presynaptic inhibitory proteins, specifically in
inhibitory-to-excitatory neuron synapses. Importantly, on a
single-cell level hNR1 antibody selectively impairs
NMDAR-mediated currents and synaptic transmission of
cortical inhibitory neurons, yet has no effect on excitatory
neurons, which contrasts with its effects on hippocampal
neurons. Together, these findings provide a novel,
cortex-specific mechanism of antibody-induced neuronal
hyperexcitability, highlighting regional specificity
underlying the pathology of autoimmune
encephalitis.SIGNIFICANCE STATEMENT It is increasingly
appreciated that the inadvertent activation of the immune
system within CNS can underlie pathogenesis of
neuropsychiatric disorders. Although the exact mechanisms
remain elusive, autoantibodies derived from patients with
autoimmune encephalitis pose a unique tool to study
pathogenesis of neuropsychiatric states. Our analysis
reveals that autoantibody against the NMDA receptor (NMDAR)
has a distinct mechanism of action in the cortex, where it
impairs function of inhibitory neurons leading to increased
cortical network excitability, in contrast to previously
described hippocampal synaptic mechanisms of information
encoding, highlighting brain regional specificity. Notably,
similar mechanism of NMDAR-mediated inhibitory hypofunction
leading to cortical disinhibition has been suggested to
underlie pathology of schizophrenia, hence our data provide
new evidence for common mechanisms underlying
neuropsychiatric disorders.},
keywords = {Autoantibodies: metabolism / Encephalitis / Hashimoto
Disease / Humans / Neurons: physiology / Receptors,
N-Methyl-D-Aspartate: metabolism / Seizures: metabolism /
NMDAR (Other) / autoantibodies (Other) / autoimmune
encephalitis (Other) / cortical interneurons (Other) /
network excitability (Other) / Autoantibodies (NLM
Chemicals) / Receptors, N-Methyl-D-Aspartate (NLM
Chemicals)},
cin = {AG Garner / AG Prüß / AG Ackermann},
ddc = {610},
cid = {I:(DE-2719)1810001 / I:(DE-2719)1810003 /
I:(DE-2719)1813004},
pnm = {351 - Brain Function (POF4-351) / 353 - Clinical and Health
Care Research (POF4-353)},
pid = {G:(DE-HGF)POF4-351 / G:(DE-HGF)POF4-353},
typ = {PUB:(DE-HGF)16},
pubmed = {pmid:35241491},
pmc = {pmc:PMC8994542},
doi = {10.1523/JNEUROSCI.1689-21.2022},
url = {https://pub.dzne.de/record/164003},
}